Vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis

Development

Volumn 133, Issue 10, 2006, Pages 1871-1880

  Herz, Hans Martin ^a   Chen, Zhihong ^b   Scherr, Heather ^b   Lackey, Melinda ^b   Bolduc, Clare ^b   Bergmann, Andreas ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Apoptosis; Cell proliferation; Cell survival; ESCRT; MVB; Notch; Protein sorting; Vps25

Indexed keywords

CELL SURFACE RECEPTOR; CYTOPLASM PROTEIN; HEAD INVOLUTION DEFECTIVE PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; JANUS KINASE; NOTCH RECEPTOR; PROTEIN VPS25; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL CLONING; CELL DEATH; CELL GROWTH; CELL MUTANT; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DROSOPHILA; ENDOSOME; ENZYME ACTIVATION; FEMALE; GENE REPRESSION; GENETIC SCREENING; HOMEOSTASIS; INHIBITION KINETICS; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

ALLELES; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CARRIER PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; DROSOPHILA; DROSOPHILA PROTEINS; ENDOSOMES; EYE; GENE EXPRESSION REGULATION; GENES, INSECT; MOSAICISM; MUTATION; PROTEIN TRANSPORT; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 33745066393     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02356     Document Type: Article

References (71)

1. Abrams, J. M. (2002). Competition and compensation: coupled to death in development and cancer. Cell 110, 403-406.
2. Adachi-Yamada, T. and O'Connor, M. B. (2002). Morphogenetic apoptosis: a mechanism for correcting discontinuities in morphogen gradients. Dev. Biol. 251, 74-90.
3. Adachi-Yamada, T., Fujimura-Kamada, K., Nishida, Y. and Matsumoto, K. (1999). Distortion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing. Nature 400, 166-169.
4. Babst, M. (2005). A protein's final ESCRT Traffic 6, 2-9.
5. Bergmann, A., Yang, A. Y. and Srivastava, M. (2003). Regulators of IAP function: coming to grips with the grim reaper. Curr. Opin. Cell Biol. 15, 717-724.
6. Brown, S., Hu, N. and Hombria, J. C. (2001). Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol. 11, 1700-1705.
7. Cashio, P., Lee, T. V. and Bergmann, A. (2005). Genetic control of programmed cell death in Drosophila melanogaster. Semin. Cell Dev. Biol. 16, 225-235.
8. Chao, J. L., Tsai, Y. C., Chiu, S. J. and Sun, Y. H. (2004). Localized Notch signal acts through eyg and upd to promote global growth in Drosophila eye. Development 131, 3839-3847.
9. de Gassart, A., Geminard, C., Hoekstra, D. and Vidal, M. (2004). Exosome secretion: the art of reutilizing nonrecycled proteins? Traffic 5, 896-903.
10. de la Cova, C., Abril, M., Bellosta, P., Gallant, P. and Johnston, L. A. (2004). Drosophila myc regulates organ size by inducing cell competition. Cell 117, 107-116.
11. Demirov, D. G. and Freed, E. O. (2004). Retrovirus budding. Virus Res. 106, 87-102.
12. Edgar, B. A. (2006). From cell structure to transcription: hippo forges a new path. Cell 124, 267-273.
13. Felder, S., Miller, K., Moehren, G., Ullrich, A., Schlessinger, J. and Hopkins, C. R. (1990). Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 61, 623-634.
14. Gonzalez-Gaitan, M. (2003). Signal dispersal and transduction through the endocytic pathway. Nat. Rev. Mol. Cell Biol. 4, 213-224.
15. Grether, M. E., Abrams, J. M., Agapite, J., White, K. and Steller, H. (1995). The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9, 1694-1708.
16. Gruenberg, J. and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323.
17. Haglund, K. and Dikic, I. (2005). Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359.
18. Hamaratoglu, F., Willecke, M., Kango-Singh, M., Nolo, R., Hyun, E., Tao, C., Jafar-Nejad, H. and Halder, G. (2006). The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat. Cell Biol. 8, 27-36.
19. Hanahan, D. and Weinberg, R. A. (2000). The hallmarks of cancer. Cell 100, 57-70.
20. Harrison, D. A., McCoon, P. E., Binari, R., Gilman, M. and Perrimon, N. (1998). Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev. 12, 3252-3263.
21. Harvey, K. F., Pfleger, C. M. and Hariharan, I. K. (2003). The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114, 457-467.
22. Hay, B. A., Wassarman, D. A. and Rubin, G. M. (1995). Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262.
23. Hicke, L. and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172.
24. Hierro, A., Sun, J., Rusnak, A. S., Kim, J., Prag, G., Emr, S. D. and Hurley, J. H. (2004). Structure of the ESCRT-II endosomal trafficking complex. Nature 431, 221-225.
25. Holley, C. L., Olson, M. R., Colon-Ramos, D. A. and Kornbluth, S. (2002). Reaper eliminates IAP proteins through stimulated IAP degradation and generalized translational inhibition. Nat. Cell Biol. 4, 439-444.
26. Huh, J. R., Guo, M. and Hay, B. A. (2004). Compensatory proliferation induced by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Curr. Biol. 14, 1262-1266.
27. Jekely, G. and Rorth, R (2003). Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4, 1163-1168.
28. Kamura, T., Burian, D., Khalili, H., Schmidt, S. L., Sato, S., Liu, W. J., Conrad, M. N., Conaway, R. C., Conaway, J. W. and Shilatifard, A. (2001). Cloning and characterization of ELL-associated proteins EAP45 and EAP20. a role for yeast EAP-like proteins in regulation of gene expression by glucose. J. Biol. Chem. 276, 16528-16533.
29. Katzmann, D. J., Odorizzi, G. and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905.
30. Krempler, A., Henry, M. D., Triplett, A. A. and Wagner, K. U. (2002). Targeted deletion of the Tsg101 gene results in cell cycle arrest at G1/ S and p53-independent cell death. J. Biol. Chem. 277, 43216-43223.
31. Kuranaga, E., Kanuka, H., Igaki, T., Sawamoto, K., Ichijo, H., Okano, H. and Miura, M. (2002). Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat. Cell Biol. 4, 705-710.
32. Le Borgne, R., Bardin, A. and Schweisguth, F. (2005). The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 132, 1751-1762.
33. Le Roy, C. and Wrana, J. L. (2005). Signaling and endocytosis: a team effort for cell migration. Dev. Cell 9, 167-168.
34. Lee, T. and Luo, L. (2001). Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254.
35. Lewis, E. B. and Bacher, F. (1968). Method of feeding ethyl methanesulfonate (EMS) to Drosophila males. Drosoph. Inf. Serv. 43, 193.
36. Li, L. and Cohen, S. N. (1996). Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85, 319-329.
37. Li, L., Li, X., Francke, U. and Cohen, S. N. (1997). The TSG101 tumor susceptibility gene is located in chromosome 11 band p15 and is mutated in human breast cancer. Cell 88, 143-154.
38. Lin, S. Y., Chen, Y. J. and Chang, J. G. (1998). Multiple truncated transcripts of TSG101 in gastrointestinal cancers. J. Gastroenterol. Hepatol. 13, 1111-1114.
39. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Permetta, G. and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269.
40. Meier, P., Silke, J., Leevers, S. J. and Evan, G. I. (2000). The Drosophila caspase DRONC is regulated by DIAP1. EMBO J. 19, 598-611.
41. Miller, D. T. and Cagan, R. L. (1998). Local induction of patterning and programmed cell death in the developing Drosophila retina. Development 125, 2327-2335.
42. Moberg, K. H., Schelble, S., Burdick, S. K. and Hariharan, I. K. (2005). Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9, 699-710.
43. Moreno, E. and Basler, K. (2004). dMyc transforms cells into super-competitors. Cell 117, 117-129.
44. Muller, P., Kuttenkeuler, D., Gesellchen, V., Zeidler, M. P. and Boutros, M. (2005). Identification of JAK/STAT signalling components by genome-wide RNA interference. Nature 436, 871-875.
45. Newsome, T. P., Asling, B. and Dickson, B. J. (2000). Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860.
46. Odorizzi, G., Babst, M. and Emr, S. D. (1998). Fab1p Ptdins(3)P 5-kinase function essential for protein sorting in the multivesicular body Cell 95, 847-858.
47. Pantalacci, S., Tapon, N. and Leopold, P. (2003). The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5, 921-927.
48. Perez-Garijo, A., Martin, F. A. and Morata, G. (2004). Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131, 5591-5598.
49. Pornillos, O., Garrus, J. E. and Sundquist, W. I. (2002). Mechanisms of enveloped RNA virus budding. Trends Cell Biol. 12, 569-579.
50. Raiborg, C., Rusten, T. E. and Stenmark, H. (2003). Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15, 446-455.
51. Raymond, C. K., Howald-Stevenson, I., Vater, C. A. and Stevens, T. H. (1992). Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402.
52. Reynolds-Kenneally, J. and Mlodzik, M. (2005). Notch signaling controls proliferation through cell-autonomous and non-autonomous mechanisms in the Drosophila eye. Dev. Biol. 285, 38-48.
53. Ryoo, H. D., Bergmann, A., Gonen, H., Ciechanover, A. and Steller, H. (2002). Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat. Cell Biol. 4, 432-438.
54. Ryoo, H. D., Gorenc, T. and Steller, H. (2004). Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev. Cell 7, 491-501.
55. Schmidt, A. E., Miller, T., Schmidt, S. L., Shiekhattar, R. and Shilatifard, A. (1999). Cloning and characterization of the EAP30 subunit of the ELL complex that confers derepression of transcription by RNA polymerase II. J. Biol. Chem. 274, 21981-21985.
56. Sen, A., Reddy, G. V. and Rodrigues, V. (2003). Combinatorial expression of Prospero, Seven-up, and Elav identifies progenitor cell types during sense-organ differentiation in the Drosophila antenna. Dev. Biol. 254, 79-92.
57. Seto, E. S. and Bellen, H. J. (2004). The ins and outs of Wingless signaling. Trends Cell Biol. 14, 45-53.
58. Srivastava, M., Scherr, M., Lackey, M., Xu, D., Chen, Z., Lu, J. and Bergmann, A. (2006). ARK, the Apaf-1 related killer in Drosophila, requires diverse domains for its apoptotic activity. Cell Death Diff. In press.
59. Sun, Z., Pan, J., Bubley, G. and Balk, S. P. (1997). Frequent abnormalities of TSG101 transcripts in human prostate cancer. Oncogene 15, 3121-3125.
60. Teo, H., Perisic, O., Gonzalez, B. and Williams, R. L. (2004). ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7, 559-569.
61. Thompson, B. J., Mathieu, J., Sung, H. H., Loeser, E., Rorth, P. and Cohen, S. M. (2005). Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711-720.
62. Tsai, Y. C. and Sun, Y. H. (2004). Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis 39, 141-153.
63. Udan, R. S., Kango-Singh, M., Nolo, R., Tao, C. and Halder, G. (2003). Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway Nat. Cell Biol. 5, 914-920.
64. Vaccari, T. and Bilder, D. (2005). The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687-698.
65. Vidal, M. and Cagan, R. L. (2006). Drosophila models for cancer research. Curr. Opin. Genet. Dev. 16, 10-16.
66. Wagner, K. U., Krempler, A., Qi, Y., Park, K., Henry, M. D., Triplett, A. A., Riedlinger, G., Rucker, I. E. and Hennighausen, L. (2003). Tsg101 is essential for cell growth, proliferation, and cell survival of embryonic and adult tissues. Mol. Cell. Biol. 23, 150-162.
67. Wu, S., Huang, J., Dong, J. and Pan, D. (2003). hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114, 445-456.
68. Xu, D., Li, Y., Arcaro, M., Lackey, M. and Bergmann, A. (2005). The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila. Development 132, 2125-2134.
69. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
70. Yoo, S. J., Huh, J. R., Muro, I., Yu, H., Wang, L., Wang, S. L., Feldman, R. M., Clem, R. J., Muller, H. A. and Hay, B. A. (2002). Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 4, 416-424.
71. Zhai, R. G., Hiesinger, P. R., Koh, T. W., Verstreken, P., Schulze, K. L., Cao, Y., Jafar-Nejad, H., Norga, K. K., Pan, H., Bayat, V. et al. (2003). Mapping Drosophila mutations with molecularly defined P element insertions. Proc. Natl. Acad. Sci. USA 100, 10860-10865.